Magnetoreception is a sense which allows an organism to detect the Earth's magnetic field. Animals with this sense include some arthropods, molluscs, and vertebrates (fish, amphibians, reptiles, birds, and mammals). The sense is mainly used for orientation and navigation, but it may help some animals to form regional maps. Experiments on migratory birds provide evidence that they make use of a cryptochrome protein in the eye, relying on the quantum radical pair mechanism to perceive magnetic fields. This effect is extremely sensitive to weak magnetic fields, and readily disturbed by radio-frequency interference, unlike a conventional iron compass. Some bacteria orient passively using magnetite crystals; the mechanism has not been reliably detected in eukaryotes.
Cartilaginous fish including sharks and stingrays can detect small variations in electric potential with their electroreceptive organs, the ampullae of Lorenzini. These appear to be able to detect magnetic fields by induction. There is some evidence that these fish use magnetic fields in navigation.
History
Biologists have long wondered whether migrating animals such as birds and sea turtles have an inbuilt magnetic compass, enabling them to navigate using the Earth's magnetic field. Until late in the 20th century, evidence for this was essentially only behavioural: many experiments demonstrated that animals could indeed derive information from the magnetic field around them, but gave no indication of the mechanism. In 1972, Roswitha and Wolfgang Wiltschko showed that migratory birds responded to the direction and inclination (dip) of the magnetic field. In 1977, M. M. Walker and colleagues identified iron-based (magnetite) magnetoreceptors in the snouts of rainbow trout. In 2003, G. Fleissner and colleagues claimed to have found iron-based receptors in the upper beaks of homing pigeons, but subsequent studies employing high resolution electron microscopy revealed that the cells identified are in fact macrophages. Research took a different direction in 2000, when Thorsten Ritz and colleagues suggested that a photoreceptor protein in the eye, cryptochrome, was a magnetoreceptor, working at a molecular scale by quantum entanglement.
Proposed mechanisms
Passive iron-based alignment in bacteria
Magnetotactic bacteria of multiple taxa contain sufficient magnetic material in the form of magnetosomes, nanometer-sized particles of iron-containing magnetite, that the Earth's magnetic field passively aligns them, just as it does with a compass needle. The bacteria are thus not actually sensing the magnetic field.
A possible but unexplored mechanism of magnetoreception in animals is through endosymbiosis with magnetotactic bacteria, whose DNA is widespread in animals. This would involve having these bacteria living inside an animal, and their magnetic alignment being used as part of a magnetoreceptive system.
While numerous studies have claimed to identify magnetite-based magneotoreceptors in vertebrates such as birds, none have been independently replicated; most have been shown to be iron-rich macrophages or environmental contaminants.
In animals
In animals, the mechanism for magnetoreception is still under investigation. Three main hypotheses are currently being discussed: one proposing a quantum compass based on a radical pair mechanism, one postulating an iron-based magnetic compass with magnetite particles, and a third that relies on electromagnetic induction.
Cryptochrome
According to the first model, magnetoreception is possible via the radical pair mechanism, which is well-established in spin chemistry. The mechanism requires two molecules, each with unpaired electrons, at a suitable distance from each other. When these can exist in states either with their spin axes in the same direction, or in opposite directions, the molecules oscillate rapidly between the two states. That oscillation is extremely sensitive to magnetic fields. Because the Earth's magnetic field is extremely weak, at 0.5 gauss, the radical pair mechanism is currently the only credible way that the Earth's magnetic field could cause chemical changes (as opposed to the mechanical forces which would be detected via magnetic crystals acting like a compass needle).
In 1978, Schulten and colleagues proposed that this was the mechanism of magnetoreception. In 2000, scientists proposed that cryptochrome – a flavoprotein in the rod cells in the eyes of birds – was the "magnetic molecule" behind this effect. It is the only protein known to form photoinduced radical-pairs in animals. The function of cryptochrome varies by species, but its mechanism is always the same: exposure to blue light excites an electron in a chromophore, which causes the formation of a radical-pair whose electrons are quantum entangled, enabling the precision needed for magnetoreception.
Many lines of evidence point to cryptochrome and radical pairs as the mechanism of magnetoreception in birds:
Despite 20 years of searching, no biomolecule other than cryptochrome has been identified capable of supporting radical pairs. In cryptochrome, a yellow molecule flavin adenine dinucleotide (FAD) can absorb a photon of blue light, putting the cryptochrome into an activated state: an electron is transferred from a tryptophan amino acid to the FAD molecule, forming a radical pair. Of the six types of cryptochrome in birds, cryptochrome-4a (Cry4a) binds FAD much more tightly than the rest. Cry4a levels in migratory birds, which rely on navigation for their survival, are highest during the spring and autumn migration periods, when navigation is most critical. The Cry4a protein from the European robin, a migratory bird, is much more sensitive to magnetic fields than similar but not identical Cry4a from pigeons and chickens, which are non-migratory.
These findings together suggest that the Cry4a of migratory birds has been selected for its magnetic sensitivity.
Behavioral experiments on migratory birds support this theory. Caged migratory birds such as robins display migratory restlessness, known by ethologists as , in spring and autumn: they often orient themselves in the direction in which they would migrate. In 2004, Thorsten Ritz showed that a weak radio-frequency electromagnetic field, chosen to be at the same frequency as the singlet-triplet oscillation of cryptochrome radical pairs, effectively interfered with the birds' orientation. The field would not have interfered with an iron-based compass. Further, birds are unable to detect a 180 degree reversal of the magnetic field, something they would straightforwardly detect with an iron-based compass.
From 2007 onwards, Henrik Mouritsen attempted to replicate this experiment. Instead, he found that robins were unable to orient themselves in the wooden huts he used. Suspecting extremely weak radio-frequency interference from other electrical equipment on the campus, he tried shielding the huts with aluminium sheeting, which blocks electrical noise but not magnetic fields. When he earthed the sheeting, the robins oriented correctly; when the earthing was removed, the robins oriented at random. Finally, when the robins were tested in a hut far from electrical equipment, the birds oriented correctly. These effects imply a radical-pair compass, not an iron one.
In 2016, Wiltschko and colleagues showed that European robins were unaffected by local anaesthesia of the upper beak, showing that in these test conditions orientation was not from iron-based receptors in the beak. In their view, cryptochrome and its radical pairs provide the only model that can explain the avian magnetic compass. A supplement to the paper summarizes alternative hypotheses on avian compass mechanisms. A scheme with three radicals rather than two has been proposed as more resistant to spin relaxation and explaining the observed behaviour better.
Electromagnetic induction
Another possible mechanism of magnetoreception in animals is electromagnetic induction in cartilaginous fish, namely sharks, stingrays, and chimaeras. These fish have electroreceptive organs, the ampullae of Lorenzini, which can detect small variations in electric potential. The organs are mucus-filled and consist of canals that connect pores in the skin of the mouth and nose to small sacs within the animal's flesh. They are used to sense the weak electric fields of prey and predators. These organs have been predicted to sense magnetic fields, by means of Faraday's law of induction: as a conductor moves through a magnetic field an electric potential is generated. In this case the conductor is the animal moving through a magnetic field, and the potential induced () depends on the time ()-varying rate of magnetic flux () through the conductor according to
The ampullae of Lorenzini detect very small fluctuations in the potential difference between the pore and the base of the electroreceptor sac. An increase in potential results in a decrease in the rate of nerve activity. This is analogous to the behavior of a current-carrying conductor. Sandbar sharks, Carcharinus plumbeus, have been shown to be able to detect magnetic fields; the experiments provided non-definitive evidence that the animals had a magnetoreceptor, rather than relying on induction and electroreceptors. Electromagnetic induction has not been studied in non-aquatic animals.
The yellow stingray, Urobatis jamaicensis, is able to distinguish between the intensity and inclination angle of a magnetic field in the laboratory. This suggests that cartilaginous fishes may use the Earth's magnetic field for navigation.
Unanswered questions
It remains likely that two or more complementary mechanisms play a role in magnetic field detection in animals. Of course, this potential dual mechanism theory raises the questions of to what degree each method is responsible for the stimulus, and how they produce a signal in response to the weak magnetic field of the Earth.
In addition, it is possible that magnetic senses may be different for different species. Some species may only be able to detect north and south, while others may only be able to differentiate between the equator and the poles. Although the ability to sense direction is important in migratory navigation, many animals have the ability to sense small fluctuations in earth's magnetic field to map their position to within a few kilometers.
Taxonomic range
Magnetoreception is widely distributed taxonomically. It is present in many of the animals so far investigated. These include arthropods, molluscs, and among vertebrates in fish, amphibians, reptiles, birds, and mammals. Its status in other groups remains unknown.
The ability to detect and respond to magnetic fields may exist in plants, possibly as in animals mediated by cryptochrome. Experiments by different scientists have identified multiple effects, including changes to growth rate, seed germination, mitochondrial structure, and responses to gravity (geotropism). The results have sometimes been controversial, and no mechanism has been definitely identified. The ability may be widely distributed, but its taxonomic range in plants is unknown.
In molluscs